Skip to main content
SpringerLink
Log in

Using genetic monitoring to inform best practice in a captive breeding programme: inbreeding and potential genetic rescue in the freshwater pearl mussel Margaritifera margaritifera

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Freshwater pearl mussel (Margaritifera margaritifera) populations are declining in Northern Ireland to the extent that a captive breeding programme was established on the Upper Ballinderry river in 1998. Previous genetic analysis of the hatchery broodstock and their first cohort of offspring showed significant levels of inbreeding (F IS  = 0.166). The broodstock, which currently numbers ca. 90 individuals, was supplemented with new individual mussels, whilst in 2013, a previously unknown population was discovered on the Lower Ballinderry river. The aim of the present study was to determine whether the rotation of the broodstock has led to a decrease in the levels of inbreeding in the second cohort of juveniles, and to determine whether the new population found in the Lower Ballinderry was genetically distinct from the captive bred population and populations from the Upper Ballinderry, which represent the source of the hatchery broodstock. Genotyping using eight microsatellite markers indicated that levels of inbreeding in the second cohort of captive-bred mussels were high, (F IS  = 0.629), and were comparable to those sampled from the original cohort and the hatchery broodstock (F IS  = 0.527 and 0.636 respectively). Bayesian analysis of population structure indicated that the newly discovered Lower Ballinderry population was genetically distinct from the broodstock and its source populations on the Upper Ballinderry. The observed differentiation was primarily due to differences in allele frequencies, and was most likely a result of genetic drift. The occurrence of ten alleles, albeit at low frequency, in the Lower Ballinderry population, including four private alleles, suggests that this new population could be incorporated into the broodstock with the aim of decreasing levels of inbreeding in the future.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alkemade R, van Oorschot M, Miles L, Nellemann C, Bakkenes M, ten Brink B (2009) GLOBIO3: a framework to investigate options for reducing global terrestrial Biodiversity loss. Ecosystems 12:374–390

    Article  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation breeding and restoration. Conservation and the genetics of populations. Blackwell, Oxford, pp 449–481

    Google Scholar 

  • Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265

    Article  CAS  PubMed  Google Scholar 

  • Baker CS, Steel D, Choi Y, Lee H, Kim KS, Choi SK, Ma Y-U, Hambleton C, Psihoyos L, Brownell RL et al (2010) Genetic evidence of illegal trade in protected whales links Japan with the US and South Korea. Biol Lett 6:647–650

    Article  PubMed  PubMed Central  Google Scholar 

  • Beasley CR, Roberts D (1996) The current distribution and status of the freshwater pearl mussel Margaritifera margaritifera L. 1758 in north-west Ireland. Aquatic Conserv: Marine and Freshwater Ecosystems 6:169–177

    Article  Google Scholar 

  • Beasley C, Roberts D (1999) Towards a strategy for the conservation of the freshwater pearl mussel Margaritifera margaritifera in County Donegal, Ireland. Biol Conserv 89:275–284

    Article  Google Scholar 

  • Beasley CR, Roberts D, Mackie TG (1998) Does the freshwater pearl mussel, Margaritifera margaritifera L., face extinction in Northern Ireland? Aquatic Conserv: Marine and Freshwater Ecosystems 8:265–272

    Article  Google Scholar 

  • Bellard C, Bertelsmeier C, Leadley P, Thuiller W, Courchamp F (2012) Impacts of climate change on the future of biodiversity. Ecol Lett 15:365–377

    Article  PubMed  PubMed Central  Google Scholar 

  • Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila. J Evol Biol 13:502–514

    Article  Google Scholar 

  • Bolland JD, Bracken LJ, Martin R, Lucas MC (2010) A protocol for stocking hatchery reared freshwater pearl mussel Margaritifera margaritifera. Aquatic Conserv: Marine and Freshwater Ecosystems 20:695–704

    Article  Google Scholar 

  • Brummett RE, Ponzoni RW (2009) Concepts, alternatives, and environmental considerations in the development and use of improved strains of Tilapia in African aquaculture. Rev Fisheries Sci 17:70–77

    Article  Google Scholar 

  • Buddensiek V (1995) The culture of juvenile freshwater pearl mussels Margaritifera margaritifera L. in cages: a contribution to conservation programmes and the knowledge of habitat requirements. Biol Conserv 74:33–40

    Article  Google Scholar 

  • Clavero M, Brotons L, Pons P, Sol D (2009) Prominent role of invasive species in avian biodiversity loss. Biodiv Conserv 142:2043–2049

    Article  Google Scholar 

  • Coleman FC, Williams SL (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends Ecol Evol 17:40–44

    Article  Google Scholar 

  • Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Crawford NG (2010) SMOGD: software for the measurement of genetic diversity. Mol Ecol Resources 10:556–557

    Article  Google Scholar 

  • Dextrase AJ, Mandrak NE (2006) Impacts of alien invasive species on freshwater fauna at risk in Canada. Biol Invasions 8:13–24

    Article  Google Scholar 

  • Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard A-H, Soto D, Stiassny MLJ et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182

    Article  PubMed  Google Scholar 

  • DOE (2005) Northern Ireland species action plan - freshwater pearl Mussel Margaritifera margaritifera. Department of Environment

  • Ebenhard T (1995) Conservation breeding as a tool for saving animal species from extinction. Trends Ecol Evol 10:438–443

    Article  CAS  PubMed  Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mole Ecol Resources 10:564–567

    Article  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  PubMed Central  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html

  • Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333

    Article  PubMed  Google Scholar 

  • Frankham R, Lees K, Montgomery ME, England PR, Lowe EH, Briscoe DA (1999) Do population size bottlenecks reduce evolutionary potential? Animal Conserv 2:255–260

    Article  Google Scholar 

  • Fraser DJ (2008) How well can captive breeding programs conserve biodiversity? A review of salmonids. Evolutionary Appl 1:535–586

    Article  Google Scholar 

  • Fredrickson RJ, Siminski P, Woolf M, Hedrick PW (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proc R Soc Lond (Biol) 274:2365–2371

    Article  Google Scholar 

  • Geist J (2010) Strategies for the conservation of endangered freshwater pearl mussels (Margaritifera margaritifera L.): a synthesis of conservation genetics and ecology. Hydrobiologia 644:69–88

    Article  Google Scholar 

  • Geist J, Kuehn R (2005) Genetic diversity and differentiation of central European freshwater pearl mussel (Margaritifera margaritifera L.) populations: implications for conservation and management. Mol Ecol 14:425–439

    Article  CAS  PubMed  Google Scholar 

  • Geist J, Rottmann O, Schröder W, Kühn R (2003) Development of microsatellite markers for the endangered freshwater pearl mussel Margaritifera margaritifera L. (Bivalvia: unionoidea). Mol Ecol Notes 3:444–446

    Article  CAS  Google Scholar 

  • Geist J, Porkka M, Kuehn R (2006) The status of host fish populations and fish species richness in European freshwater pearl mussel (Margaritifera margaritifera) streams. Aquat Conserv Mar Freshwater Ecosyst 16:251–266

    Article  Google Scholar 

  • Habitas (2006) Northern Ireland’s priority species. http://www.habitas.org.uk/priority/

  • Hastie LC, Cooksley SL, Scougall F, Young MR, Boon PJ, Gaywood MJ (2003) Characterization of freshwater pearl mussel (Margaritifera margaritifera) riverine habitat using River Habitat Survey data. Aquat Conserv Mar Freshwater Ecosyst 13:213–224

    Article  Google Scholar 

  • Hedrick PW (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636

    Article  Google Scholar 

  • Hedrick PW (2005) Genetic restoration:’ a more comprehensive perspective than ‘genetic rescue. Trends Ecol Evol 20:109

    Article  PubMed  Google Scholar 

  • Hedrick PW, Fredrickson R (2010) Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv Genet 11:615–626

    Article  Google Scholar 

  • Henley WF, Grobler PJ, Neves RJ (2006) Non-invasive method to obtain DNA from freshwater mussels (Bivalvia: unionidae). J Shellfish Res 25:975–977

    Article  Google Scholar 

  • Horton M, Keys A, Kirkwood L, Mitchell F, Kyle R, Roberts D (2015) Sustainable catchment restoration for reintroduction of captive bred freshwater pearl mussels Margaritifera margaritifera. Limnologica 50:21–28

    Article  Google Scholar 

  • Jackson JA, Laikre L, Baker CS, Kendall KC (2012) Guidelines for collecting and maintaining archives for genetic monitoring. Conserv Genet Resources 4:527–536

    Article  Google Scholar 

  • Jones JW, Hallerman EM, Neves RJ (2006) Genetic management guidelines for captive propagation of freshwater mussels (Unionoidea). J Shellfish Res 25:527–535

    Article  Google Scholar 

  • JNCC (2007) The convention on the conservation of European wildlife and natural habitats. http://jncc.defra.gov.uk/page-1364

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Karlsson S, Larsen BM, Eriksen L, Hagan M (2013) Four methods of nondestructive DNA sampling from freshwater pearl mussels Margaritifera margaritifera L. (Bivalvia: unionoida). Freshwat Sci 32:525–530

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kingsford RT, Watson JEM, Lundquist CJ, Venter O, Hughes L, Johnston EL, Atherton J, Gawel M, Keith DA, Mackey BG et al (2009) Major conservation policy issues for biodiversity in Oceania. Conserv Biol 23:834–840

    Article  CAS  PubMed  Google Scholar 

  • Kohn MH, Murphy WJ, Ostrander EA, Wayne RK (2006) Genomics and conservation genetics. Trends Ecol Evol 21:629–637

    Article  PubMed  Google Scholar 

  • Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussaari M, Lindborg R, Ockinger E, Pärtel M, Pino J et al (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605

    Article  PubMed  PubMed Central  Google Scholar 

  • Kubota H, Watananbe K, Suguro N, Tabe M, Umezawa K, Watanabe S (2010) Genetic population structure and management units of the endangered Tokyo bitterling, Tanakia tanago (Cyprinidae). Conserv Genet 11:2343–2355

    Article  Google Scholar 

  • Lacy RC, Petric A, Warneke M (1993) Inbreeding and outbreeding in captive populations of wild animal species. The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. University of Chicago Press, Chicago, pp 352–374

    Google Scholar 

  • Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 7:295–302

    Article  Google Scholar 

  • Luoto M, Rekolainen S, Aakkula J, Pykälä J (2003) Loss of plant species richness and habitat connectivity in grasslands associated with agricultural change in Finland. Ambio 32:447–452

    Article  PubMed  Google Scholar 

  • Mace GM, Baillie JEM (2007) The 2010 biodiversity indicators: challenges for science and policy. Conserv Biol 21:1406–1413

    Article  PubMed  Google Scholar 

  • McKelvey KS, Von Kienast J, Aubry KB, Koehler GM, Maletzke BT, Squires JR, Lindquist EL, Loch S, Schwartz MK (2006) DNA analysis of hair and scat collected along snow tracks to document the presence of Canada lynx. Wildlife Soc Bull 34:451–455

    Article  Google Scholar 

  • McPhee M (2004) Generations in captivity increases behavioral variance: considerations for captive breeding and reintroduction programs. Biol Conserv 115:71–77

    Article  Google Scholar 

  • Mortiz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130:217–228

    Article  Google Scholar 

  • Österling ME, Arvidsson BL, Greenberg LA (2010) Habitat degradation and the decline of the threatened mussel Margaritifera margaritifera: influence of turbidity and sedimentation on the mussel and its host. J Appl Ecol 47:759–768

    Article  Google Scholar 

  • Paxton RJ, Thoren PA, Tengo J, Estoup A, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511–519

    Article  CAS  PubMed  Google Scholar 

  • Preston SJ, Keys A, Roberts D (2007) Culturing freshwater pearl mussel Margaritifera margaritifera: a breakthrough in the conservation of an endangered species. Aquat Conserv Mar Freshwater Ecosyst 17:539–549

    Article  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Reid N, Keys A, Preston JS, Moorkens E, Roberts D, Wilson CD (2013) Conservation status and reproduction of the critically endangered freshwater pearl mussel (Margaritifera margaritifera) in Northern Ireland. Aquat Conserv Mar Freshwater Ecosyst 23:571–581

    Article  Google Scholar 

  • Reis J (2003) The freshwater pearl mussel (Margaritifera margaritifera L.) (Bivalvia, Unionoida) rediscovered in Portugal and threats to its survival. Biol Conserv 114:447–452

    Article  Google Scholar 

  • Robert A (2009) Captive breeding genetics and reintroduction success. Biodiv Conserv 142:2915–2922

    Article  Google Scholar 

  • Saunders DL, Meeuwig JJ, Vincent ACJ (2002) Freshwater protected areas: strategies for conservation. Conserv Biol 16:30–41

    Article  Google Scholar 

  • Scheder C, Gumpinger C (2008) The freshwater pearl mussel (Margaritifera margaritifera Linne, 1758) in Upper Austria- A species treatened with extinction and current measures for its sustained protection. Romanian J Biol: Zoological 52:52–59

    Google Scholar 

  • Scheder C, Lerchegger B, Jung M, Csar D, Gumpinger C (2014) Practical experience in the rearing of freshwater pearl mussels (Margaritifera margaritifera): advantages of a work-saving infection appraoch, survival, and growth of early life stages. Hydrobiologia 735:203–212

    Article  Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2006) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33

    Article  PubMed  Google Scholar 

  • Seddon PJ, Armstrong DP, Maloney RF (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312

    Article  PubMed  Google Scholar 

  • Shen F, Zhang Z, He W, Yue B, Zhang A, Zhang L, Hou R, Wang C, Watanabe T (2009) Microsatellite variability reveals the necessity for genetic input from wild giant pandas (Ailuropoda melanoleuca) into the captive population. Mol Ecol 18:1061–1070

    Article  CAS  PubMed  Google Scholar 

  • Snyder NFR, Derrickson SR, Beissinger SR, Wiley JW, Smit TB, Toone WD, Miller B (1996) Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338–348

    Article  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statisitcs for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wilson CD (2010) Empirical approaches to the conservation of Margaritifera margaritifera. PhD thesis, Queen’s University Belfast, Belfast

  • Wilson CD, Beatty GE, Bradley CR, Clarke HC, Preston SJ, Roberts D, Provan J (2012) The importance of population genetic information in formulating ex situ conservation strategies for the freshwater pearl mussel (Margaritifera margaritifera L.) in Northern Ireland. Animal Conserv 15:593–602

    Article  Google Scholar 

  • Zippel K, Johnson K, Gagliardo R, Gibson R, McFadden M, Browne R, Martinez C, Townsend E (2011) The amphibian ark: a global community for ex situ conservation of amphibians. Herpetol Conserv Biol 6:340–352

    Google Scholar 

Download references

Acknowledgements

The authors would like to thank the staff at Ballinderry Rivers Trust (David Bell, Mark Horton, Alan Keys, Lisa Kirkwood and Frank Mitchell) and Dr. Jane Preston for their help with surveying and the time consuming job of extraction of haemolymph from the mussels and for preparing the maps. All maps in this paper are based on information provided by the Northern Ireland Environment Agency. This material is based upon Crown Copyright and is reproduced with the permission of Land & Property Services under delegated authority from the Controller of Her Majesty’s Stationery Office, Crown copyright and database rights, EMOU206.2. Northern Ireland Environment Agency Copyright 2015. Rebecca Kyle’s PhD is funded by the Department for Education and Learning, Northern Ireland, and the Northern Ireland Environment Agency. Finally, we are grateful to the Editor and to two anonymous Reviewers for helpful comments on the original version of the manuscript.

Author information

Authors and Affiliations

  1. School of Biological Sciences, Queen’s University Belfast, 97 Lisburn Road, Belfast, BT9 7BL, UK

    Rebecca Kyle, Gemma E. Beatty, Dai Roberts & Jim Provan

  2. Quercus, School of Biological Sciences, Queen’s University Belfast, 97 Lisburn Road, Belfast, BT9 7BL, UK

    Rebecca Kyle, Gemma E. Beatty, Dai Roberts & Jim Provan

  3. School of Education and Lifelong Learning, Aberystwyth University, Aberystwyth, SY23 3UX, UK

    Gemma E. Beatty

  4. Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Aberystwyth, SY23 3DA, UK

    Jim Provan

Authors
  1. Rebecca Kyle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gemma E. Beatty
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dai Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jim Provan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jim Provan.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 16 kb)

Supplementary material 2 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kyle, R., Beatty, G.E., Roberts, D. et al. Using genetic monitoring to inform best practice in a captive breeding programme: inbreeding and potential genetic rescue in the freshwater pearl mussel Margaritifera margaritifera . Conserv Genet 17, 1323–1332 (2016). https://doi.org/10.1007/s10592-016-0864-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0864-z

Keywords

Search

Navigation